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The Journal of Neurophysiology Vol. 82 No. 4 October 1999, pp. 1786-1792
Copyright ©1999 by the American Physiological Society
1Laboratory for Neuronal Recognition
Molecules,
Kashiwadani, Hideki,
Yasnory F. Sasaki,
Naoshige Uchida, and
Kensaku Mori.
Synchronized Oscillatory Discharges of Mitral/Tufted Cells With
Different Molecular Receptive Ranges in the Rabbit Olfactory Bulb.
J. Neurophysiol. 82: 1786-1792, 1999.
Individual glomeruli in the mammalian olfactory bulb represent
a single or a few type(s) of odorant receptors. Signals from different
types of receptors are thus sorted out into different glomeruli. How
does the neuronal circuit in the olfactory bulb contribute to the
combination and integration of signals received by different glomeruli?
Here we examined electrophysiologically whether there were functional
interactions between mitral/tufted cells associated with different
glomeruli in the rabbit olfactory bulb. First, we made simultaneous
recordings of extracellular single-unit spike responses of
mitral/tufted cells and oscillatory local field potentials in the
dorsomedial fatty acid-responsive region of the olfactory bulb in
urethan-anesthetized rabbits. Using periodic artificial inhalation, the
olfactory epithelium was stimulated with a homologous series of
n-fatty acids or n-aliphatic aldehydes.
The odor-evoked spike discharges of mitral/tufted cells tended to
phase-lock to the oscillatory local field potential, suggesting that
spike discharges of many cells occur synchronously during odor
stimulation. We then made simultaneous recordings of spike discharges
from pairs of mitral/tufted cells located 300-500 µm apart and
performed a cross-correlation analysis of their spike responses to odor
stimulation. In ~27% of cell pairs examined, two cells with distinct
molecular receptive ranges showed synchronized oscillatory discharges
when olfactory epithelium was stimulated with one or a mixture of
odorant(s) effective in activating both. The results suggest that the
neuronal circuit in the olfactory bulb causes synchronized spike
discharges of specific pairs of mitral/tufted cells associated with
different glomeruli and the synchronization of odor-evoked spike
discharges may contribute to the temporal binding of signals derived
from different types of odorant receptor.
To cope with a huge variety of odor molecules, the
mammalian olfactory system expresses ~500-1,000 types of odorant
receptor in the sensory neurons of the olfactory epithelium
(Buck and Axel 1991 In the large repertoire of odorant receptors, individual olfactory
sensory neurons most probably express just one type (Malnic et
al. 1999
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
; Lancet and Ben-Arie
1993; Mombaerts 1999; Sullivan et al. 1996). Because a particular object like a rose, for example,
emits dozens of specific odor molecules, their nasal inhalation
activates a specific combination of many odorant receptors. Perception
of the olfactory image of objects therefore requires that the central olfactory system either combines or compares responses across the
numerous types of odorant receptor. However, the neuronal mechanisms
for integrating signals from different receptors are not yet known.
). Thousands of olfactory sensory neurons expressing a
given odorant receptor project their axons (olfactory axons) selectively to only a few defined glomeruli in the main olfactory bulb
(MOB; Fig. 1) (Mombaerts et al.
1996; Ressler et al. 1994; Vassar et al.
1994). Thus an individual glomerulus is thought to be a
functional unit representing a single type (or a few types) of odorant
receptor. Within the glomerulus, olfactory axons make excitatory
synaptic connections with dendritic tufts of mitral and tufted cells,
which are principal neurons of the MOB. Individual mitral/tufted cells
project a single primary dendrite to a single glomerulus. Therefore
signals from different types of odorant receptor are sorted into
different glomeruli and transmitted to different mitral/tufted cells
(Fig. 1). In support of the hypothesis that individual glomeruli
represent a single odorant receptor, we have demonstrated elsewhere
that individual mitral/tufted cells associated with a single glomerulus
are tuned to specific features of odor molecules (Imamura et al.
1992; Katoh et al. 1993; Mori et al.
1992; Mori and Yoshihara 1995). The olfactory
"identity" of a given object is therefore thought to be coded by a
specific combination of activated glomeruli.
View larger version (27K):
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Fig. 1.
Schematic diagram illustrating the basic neuronal circuit of the main
olfactory bulb and the arrangement of recording micropipettes.
Olfactory sensory neurons (S) expressing the same odorant receptor
converge their axons onto a few defined glomeruli and make synaptic
terminals on dendrites of mitral cells (M), tufted cells, and
periglomerular cells (PG). Individual mitral/tufted cells project a
single primary dendrite to a single glomerulus. Mitral/tufted cells
form dendrodendritic reciprocal synapses (black and white arrows) with
granule cells (G) in the external plexiform layer (EPL), and with PG
cells in the glomeruli. GL, glomerular layer; GRL, granule cell layer;
LOT, lateral olfactory tract; MCL, mitral cell layer; MOB, main
olfactory bulb; OE, olfactory epithelium.
Stimulation of the olfactory epithelium with a mixture of odorous
compounds or even with a single compound causes activation of glomeruli
and mitral/tufted cells that are in many cases distributed over several
discrete regions of the MOB (Mori and Yoshihara 1995; Shepherd 1994; Stewart et al. 1979). In
addition, the inhalation of odor molecules elicits a prominent
oscillation (30-80 Hz) of local field potentials in the MOB,
suggesting that many mitral/tufted cells respond with synchronized
spike discharges to the odor stimulation (see, for example,
Adrian 1950; Bressler 1987;
Bressler and Freeman 1980; Mori et al.
1992; Mori and Takagi 1977). Analysis of the oscillatory local field potential (OLFP) indicated that dendrodendritic reciprocal synaptic interactions between mitral/tufted cells and granule cells are responsible for generating the OLFP in the MOB (Mori and Takagi 1977; Rall et al. 1966;
Shepherd and Greer 1990). These observations raise the
possibility that, during odor stimulation, synchronized spike responses
may occur in a number of mitral/tufted cells associated with a specific
subset of glomeruli representing a selective combination of odorant receptors.
Because the transient synchronization of spike responses might
contribute to temporal binding of input signals from different receptors as suggested by studies of the mammalian visual and somatosensory systems (Gray et al. 1989; Murthy
and Fetz 1996; Singer and Gray 1995) and the
insect olfactory system (Laurent 1996; Wehr and
Laurent 1996), we examined electrophysiologically whether odor
stimulation causes synchronous oscillatory discharges in mitral/tufted
cells of the MOB. We first examined the temporal relationship between
the spike discharges of individual mitral/tufted cells and the phase of
oscillation of the OLFP during odor stimulation. We then made
recordings of single-unit spike discharges simultaneously from pairs of
mitral/tufted cells that were located 300-500 µm apart. After
establishing the molecular receptive range (MRR) properties of each
cell, we performed a cross-correlation analysis of their spike
responses to odor stimulation.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Experiments were performed on 17 male adult rabbits (1.8-2.5
kg, Japanese White, Nihon SLC, Hamamatsu) anesthetized with urethan (1.3 g/kg). Methods for surgical preparation, artificial inhalation of
odor-containing air into the nose, stimulation with odor molecules are
described in detail in a previous paper (Imamura et al.
1992). Briefly, double tracheal cannulation was performed, one
cannula being used for respiration and the other for artificial
inhalation of odor-containing air. The cerebrospinal fluid was drained
via the atlantooccipital membrane to minimize brain pulsation. All procedures involving animal preparation were approved by the RIKEN Brain Science Institute Animal Committee.
We used a homologous series of normal (n)-fatty
acids (carbon chain length: 2-9) and n-aliphatic aldehydes
(carbon chain length: 3-10) for odor stimulation. Each odor molecule
was diluted to 2 × 10
2 (vol/vol) in
odorless mineral oil and stored in a glass test tube sealed with a
screw cap. For odor stimulation, the test tube was uncapped and then
placed in front of the animal's nose. The rate of artificial
inhalation (500 ms in duration) was maintained at once per 1.5 s.
Each odor stimulation lasted 5 s covering 3 cycles of the
artificial inhalation.
OLFPs and single-unit discharges were recorded from the dorsomedial
region of the MOB using glass micropipettes filled with 2 M NaCl. DC
resistance of the micropipettes was 1-2 M
for OLFP and 3-5 M
for extracellular recording of single-unit spikes. A pair of stainless
steel needles was inserted into the lateral olfactory tract (LOT) for
electrical stimulation (100 µs in duration). The configuration of the
LOT-evoked field potential was used for monitoring the position of the
tip of the recording micropipettes in the MOB. For simultaneous
recording of OLFP and single-unit discharges of a mitral/tufted cell,
we used two micropipettes separated at their tips ~100 µm. For
simultaneous recording from two mitral/tufted cells, the tips of two
micropipettes were separated at their tips 300-500 µm apart. The
action potentials and OLFPs were differentially amplified using
band-pass filters in the range of 150 Hz to 3 kHz and 5-300 Hz,
respectively. The recorded signals were stored in the computer
(PowerMac 7300) via AD converter with Spike 2 software (Cambridge
Electronic Design, Cambridge, UK), and further off-line analyses were performed.
For each pair of mitral/tufted cells, cross-correlation histograms
(binwidth of 2 ms) of spike discharges were calculated using a standard
method. We fitted a Gabor function {damped sinusoid: F(t) = A
exp[
(|t 
|/
)2]
cos [2
(t )] + C} to each
cross-correlogram using 
2 measurement and
determined five parameters (A, the center peak amplitude;
C, the offset of the correlogram modulation; , the phase
shift; , decay constant; , the sinusoid frequency). For estimation of the strength of cross-correlation, we calculated the
relative modulatory amplitude (RMA) defined as the ratio of the center
peak amplitude (A) over the offset of correlogram modulation (C) (Engel et al. 1990; König
1994). Spike responses were considered synchronous when the RMA
exceeded 0.3.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Spike discharges of mitral/tufted cells phase-locked to oscillatory local field potentials
Stimulation of olfactory epithelium with fatty acids of short
carbon chain elicits a prominent OLFP in the dorsomedial region of the
rabbit MOB (Mori et al. 1992). As a first step to
examine the possible synchronous firing of mitral/tufted cells, we
examined the temporal relationship between spike discharges of
mitral/tufted cells and the oscillation phases of OLFP in the
dorsomedial region of the MOB in urethan-anesthetized rabbits. Two
micropipettes were inserted into the dorsomedial region of the MOB: one
for recording OLFP in the external plexiform layer (EPL) and the other for recording extracellular single-unit spikes of mitral/tufted cells
in the mitral cell layer or the EPL (Fig. 1).
Figure 2A shows an example of
simultaneous recordings of single-unit discharges (trace 2)
and the OLFP (trace 3). Inhalation of enanthic acid
[CH3(CH2)5COOH:
C(7)-COOH] elicited a train of spike discharges of this mitral/tufted
cell and a prominent sinusoidal (~37.6 Hz) OLFP. The spike discharges
started before the beginning of OLFP and tended to phase-lock to OLFP
during the period of large oscillation. Observation with faster sweep
speeds showed that the spike discharges occurred mostly at the falling
phase of the OLFP. To examine the temporal relationship in more detail, each cycle (360°) of the OLFP was divided into 12 different phases at
30° intervals starting from the peak of positivity as 0° (top panel in Fig. 2B), and the probability of spike
discharge occurrence was plotted against the different phases of the
OLFP (phase-frequency plotting, bottom panel in Fig.
2B). In the mitral/tufted cell shown in Fig. 2B,
~91% of spike discharges occurred during the falling phases (between
0 and 180°) of the OLFP. Such detailed analysis of the temporal
relationship was performed in 15 mitral/tufted cells sampled in the
dorsomedial region, and 11 cells (~73% of cells analyzed) clearly
showed spike discharges locked to the falling phase of the OLFP. An
average histogram obtained from the 11 cells (Fig. 2C)
indicated that most of the spike discharges occurred during the period
between 0 and 150° with a peak between 60 and 90°. These results
suggest that a number of fatty acid-responsive mitral/tufted cells in
the dorsomedial region elicit their spikes synchronously during odor
stimulation. However, the phase-locking of spikes to OLFP does not
necessarily indicate spike synchronization because mitral/tufted cells
show diverse temporal patterns of odor-evoked spike discharges
(Imamura et al. 1992; Mori et al. 1992).
|
Simultaneous recording of spike discharges from a pair of mitral/tufted cells
To examine the synchronous discharges more directly, we made
simultaneous recordings from two mitral/tufted cells in the dorsomedial region of the MOB. A previous study with horseradish peroxidase labeling (Buonviso et al. 1991) has shown in rat that
cell bodies of almost all pairs of mitral cells innervating the same
glomerulus are separated by <120 µm, which corresponds to the
average diameter of a glomerulus (127 µm) (Royet et al.
1989). To minimize the possibility of recording from two
mitral/tufted cells innervating a same glomerulus, we separated the
tips of the two recording microelectrodes by >300 µm, that is,
~1.6 times greater than the average diameter (190 µm) of a
glomerulus in rabbit (Allison and Warwick 1949).
Mitral/tufted cells extend their secondary dendrites tangentially
~850 µm (Mori et al. 1983) and form numerous
dendrodendritic synapses with granule cells. To increase the
possibility of encountering mitral/tufted cells that interact with each
other via dendrodendritic synapses, the tips of two microelectrodes
were separated by up to 500 µm. Based on the above estimations, we
aimed to record from two mitral/tufted cells located between 300 and
500 µm apart.
Previous studies show spatially overlapping distributions of
mitral/tufted cells having distinct tuning patterns to fatty acids and
aliphatic aldehydes (Imamura et al. 1992; Mori et
al. 1992). This suggests that mitral/tufted cells innervating
different glomeruli interact with each other via the local neuronal
circuit and show synchronized spike discharges when they are
simultaneously activated by one or a mixture of n-fatty
acids and/or n-aliphatic aldehydes. Figure
3A shows an example of
simultaneous recordings from two mitral/tufted cells in the dorsomedial
region. When the nasal epithelium was stimulated with caproic acid
[C(6)-COOH], both cells showed burst discharges during the inhalation
of odor-containing air (Fig. 3A, trace 3 and trace
4). Observation with a faster sweep speed (Fig. 3B)
showed that spiking of the two cells tended to occur synchronously
(indicated by arrows) during the late portion of the burst discharges.
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Cross-correlation analysis of spike discharges
To further examine the synchronized spike responses, we made
simultaneous recordings from two mitral/tufted cells, determined the
MRRs of both cells using a homologous series of n-fatty
acids and n-aliphatic aldehydes, and then examined whether
the two cells fire synchronously using cross-correlation analysis of
their spike discharges. Figure 4 shows an
example of the results obtained from simultaneous recordings from two
mitral/tufted cells. MRR of one cell (S12-2) covered C(3)-
and C(4)-fatty acids (COOH; enclosed by - - -; Fig. 4A),
whereas that of the other cell (S12-1) covered C(2)- to
C(5)-COOH and C(3)- to C(5)-aliphatic aldehydes (CHO; enclosed by 
).
Because of the overlapping MRRs of the two cells, stimulation with
C(3)-COOH elicited burst spike discharges of both cells. A
cross-correlation histogram calculated for spike discharges evoked by
C(3)-COOH showed a clear central peak at the time lag of 3 ms (Fig.
4B) indicating synchronization. The spikes of the cell
S12-2 typically occurred between 2 ms before and 8 ms after
the spike of S12-1. Cross-correlation analysis (Fig.
4B) together with autocorrelation analysis (data not shown) also showed the oscillatory nature of spike discharges at a frequency of ~36 Hz. It should be noted that the synchronized oscillatory spike
discharges of the two cells occurred only during the inhalation of
odor-containing air: without odor stimulation the spike discharges of
the two cells did not show synchronization (bottom histogram of Fig. 4B).
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Cross-correlation analysis was performed on 37 pairs of mitral/tufted cells recorded in the dorsomedial region simultaneously activated by one or a mixture of odor molecules. A clear synchronization (RMA > 0.3; see METHODS) of spike discharges was observed in 10 pairs (27%) of mitral/tufted cells. In all the pairs except for one in which the determination of MRR was not completed, the MRR of one cell differed significantly from that of the other cell. In three pairs including the pair shown in Fig. 4A, the MRR of one cell was much larger and completely involved that of the other cell. In four pairs of mitral/tufted cells, the two cells showed distinct but partially overlapping MRRs as exemplified in Fig. 5A. In two pairs of mitral/tufted cells, there was no overlap of MRRs (e.g., cell pair shown in Fig. 5B).
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In the mitral/tufted cell pair shown in Fig. 5A, the overlap of MRR occurred on C(5)- and C(6)-COOH. Thus simultaneous activation of both cells was obtained by stimulation of the olfactory epithelium with either C(5)-COOH or C(6)-COOH. Cross-correlation analysis of their spike responses showed that C(5)-COOH induced a clear synchronization of spike discharges with a mean time lag of 5 ms (Fig. 5A), whereas C(6)-COOH induced weaker synchronization (data not shown). In the pair shown in Fig. 5B, the MRR of two cells showed no overlap. Therefore a mixture of odor molecules [C(5)-CHO and C(7)-CHO] was applied to the nose to activate both cells simultaneously. As shown in Fig. 5B, the cross-correlation histogram showed a robust synchronization of spike discharges with a mean time lag of 2 ms during odor stimulation. In all the pairs analyzed, the temporal nature of synchronization was evident; the synchronization was elicited only during the inhalation of odor molecules, and no synchronization was observed during the period before the odor stimulation (bottom histograms of Fig. 5, A and B).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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A number of previous studies (e.g., Adrian 1950;
Bressler 1987; Bressler and Freeman 1980;
Mori et al. 1992; Mori and Takagi 1977)
demonstrated a robust OLFP in the MOB, suggesting that many mitral/tufted cells fire in synchrony during odor stimulation. However,
detailed analyses of the temporal relationship of spike discharges of
mitral/tufted cells at high time resolutions in milliseconds have never
before been made. In this study we show that spike discharges of many
mitral/tufted cells are phase-locked to the OLFP. Furthermore, we
applied cross-correlation analysis to spike discharges of pairs of
mitral/tufted cells and show that in selective pairs, synchronous spike
discharges occur within a mean time lag of <5 ms.
Because the tips of the two recording microelectrodes were >300 µm apart, two mitral/tufted cells that were simultaneously recorded presumably innervate different glomeruli. This idea is supported by the observation that in all pairs, the MRR of one cell differed significantly from that of the other cell. The present results thus suggest that in specific pairs of mitral/tufted cells, each associated with a distinct glomerulus, activation of both cells by odor stimulation causes synchronized oscillatory spike discharges during odor stimulation. In view of the evidence that different glomeruli represent different odorant receptors, the results described above suggest that pairs of mitral/tufted cells each receiving different odorant receptor inputs show synchronized spike discharges during odor stimulation.
The function of synchronized spike discharges in the olfactory bulb is
not yet known. On the basis of observations in other sensory systems,
however, it can be speculated that this synchronization provides a
basis for the integration at the level of olfactory cortex of signals
originated from different odorant receptors. If axons of the two
mitral/tufted cells were to converge on the same target neuron in the
olfactory cortex, the synchronization of spike discharges may greatly
increase the probability of driving the target neuron because of
temporal summation of synaptic inputs from the two cells. OLFPs with
similar frequencies have been reported in the olfactory cortex
(Bressler 1987; Bressler and Freeman
1980), suggesting that synaptic inputs from the MOB occur
synchronously in the olfactory cortex. In this way, synchronization of
spike discharges of mitral/tufted cells may contribute to combining signals derived from different odorant receptors at the level of the
olfactory cortex. Extension of the present study to include analysis of
olfactory cortical neurons thus might provide us with a clue for
understanding cellular mechanisms for the integration and decoding in
the olfactory cortex of odor information that is represented by spatial
and temporal patterns of mitral/tufted cell activity.
What is the mechanism for such a precise synchronization of spike
discharges of mitral/tufted cells? Mitral/tufted cells form dendrodendritic reciprocal synapses with local inhibitory neurons, granule cells, and perigromerular cells (Fig. 1). The local neuronal circuit via these interneurons is thought to mediate functional interactions among mitral/tufted cells. Previous studies also suggest a
model in which dendrodendritic synaptic interactions with granule cells
provide the basis for the generation of rhythmic oscillatory activity
of mitral/tufted cells during odor stimulation (Mori and Takagi
1977; Rall and Shepherd 1968; Rall et al.
1966; Shepherd and Greer 1990). According to
this model, initial spike discharges of mitral/tufted cells in response
to excitatory postsynaptic potentials (EPSPs) from olfactory axon
synchronously activate mitral/tufted-to-granule dendrodendritic
excitatory synapses. The depolarization generated in granule cell
dendrites by the excitatory synaptic input causes negativity of the
OLFP in the EPL. The activated granule cells then synchronously inhibit
mitral/tufted cells via granule-to-mitral/tufted dendrodendritic
inhibitory synapses, resulting in the synchronous cessation of spike
discharges of mitral/tufted cells. When the inhibition subsides, the
long-lasting EPSPs from olfactory axons restimulate mitral/tufted cell
spike discharges. In this way many mitral/tufted cells show
synchronized oscillatory spike discharges. In the insect olfactory
system, blockade of GABA-mediated inhibition in the antennal lobe,
which is the counterpart of the mammalian olfactory bulb, has also been shown to impair the generation of the OLFPs in the mushroom body (MacLeod and Laurent 1996).
The results of the present study agree well with such a model
demonstrating that the dendrodendritic reciprocal synapses are responsible for the synchronization of mitral/tufted cells. In our own
study the distance between the two mitral/tufted cells recorded was
<500 µm, so they might interact with each other via the
dendrodendritic synaptic circuit because of the possible overlap of the
territories of their secondary dendrites. Furthermore spike discharges
of mitral/tufted cells occurred in the falling phase of the OLFP just
before the negativity, indicating the synaptic depolarization of
granule cell dendrites (Rall and Shepherd 1968). Mechanisms other than that connected with the dendrodendritic synapses
between mitral/tufted cells and granule cells may also be involved in
the generation of the synchronized oscillatory spike discharges. For
example, the synchronization might be mediated by dendrodendritic
synaptic connections with periglomerular cells, or by the local circuit
via axon collaterals of mitral/tufted cells.
In the present study, synchronization of spike discharges was observed
only in 27% of pairs examined in the dorsomedial region; the rest did
not show clear synchronization. This suggests that synchronization
occurs only in specific pairs of mitral/tufted cells. In addition, this
raises the possibility that strong dendrodendritic synaptic connections
via granule cells that result in synchronized spike discharges are
formed among specific subsets of mitral/tufted cells associated with
selective subsets of odorant receptors. Because previous studies have
suggested a plastic nature of the dendrodendritic synaptic connections
both in the accessory and main olfactory bulbs (Brennan and
Keverne 1997; Kaba and Nakanishi 1995), the
present findings might be extended to hypothesize that the degree of
synchronization among specific subsets of mitral/tufted cells might
change in response to the history of previous olfactory inputs. In
other words, a plastic change in the dendrodendritic synaptic
interactions might result in a change in the strength of temporal
binding of signals originating from different odorant receptors. The
present method of examining synchronization of spike activities of
mitral/tufted cells with defined MRR properties provides a means for
examining the above hypothesis.
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ACKNOWLEDGMENTS |
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We thank Dr. M. W. Miller of The Institute of Physical and Chemical Research (RIKEN) for a critical reading of the manuscript; Drs. H. Nagao, L. Masuda-Nakagawa, M. Yamaguchi, and H. von Campenhausen of RIKEN, and Drs. F. Murakami and N. Yamamoto of Osaka University, for a number of helpful suggestions; and K. Aijima of RIKEN for excellent technical assistance.
This work was supported in part by grants from the Ministry of Education, Science, Sports and Culture of Japan and the Human Frontier Science Program. H. Kashiwadani was supported by a grant from the Junior Research Associate Program in RIKEN, and N. Uchida was supported by the Special Postdoctoral Researchers Program, RIKEN.
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FOOTNOTES |
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Address for reprint requests: K. Mori, Laboratory for Neuronal Recognition Molecules, Brain Science Institute RIKEN, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 26 April 1999; accepted in final form 28 June 1999.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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I. G. Davison and L. C. Katz Sparse and Selective Odor Coding by Mitral/Tufted Neurons in the Main Olfactory Bulb J. Neurosci., February 21, 2007; 27(8): 2091 - 2101. [Abstract] [Full Text] [PDF]
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T. Ishikawa, T. Sato, A. Shimizu, K.-I. Tsutsui, M. de Curtis, and T. Iijima Odor-Driven Activity in the Olfactory Cortex of an In Vitro Isolated Guinea Pig Whole Brain With Olfactory Epithelium J Neurophysiol, January 1, 2007; 97(1): 670 - 679. [Abstract] [Full Text] [PDF]
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 P. A Brennan and K. M Kendrick Mammalian social odours: attraction and individual recognition Phil Trans R Soc B, December 29, 2006; 361(1476): 2061 - 2078. [Abstract] [Full Text] [PDF]
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N. E. Schoppa AMPA/Kainate Receptors Drive Rapid Output and Precise Synchrony in Olfactory Bulb Granule Cells J. Neurosci., December 13, 2006; 26(50): 12996 - 13006. [Abstract] [Full Text] [PDF]
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D. Rinberg, A. Koulakov, and A. Gelperin Sparse odor coding in awake behaving mice. J. Neurosci., August 23, 2006; 26(34): 8857 - 8865. [Abstract] [Full Text] [PDF]
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D. B. Rubin and T. A. Cleland Dynamical Mechanisms of Odor Processing in Olfactory Bulb Mitral Cells J Neurophysiol, August 1, 2006; 96(2): 555 - 568. [Abstract] [Full Text] [PDF]
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M. J. Lehmkuhle, R. A. Normann, and E. M. Maynard Trial-by-Trial Discrimination of Three Enantiomer Pairs by Neural Ensembles in Mammalian Olfactory Bulb J Neurophysiol, March 1, 2006; 95(3): 1369 - 1379. [Abstract] [Full Text] [PDF]
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 A. Kepecs, N. Uchida, and Z. F. Mainen The Sniff as a Unit of Olfactory Processing Chem Senses, February 1, 2006; 31(2): 167 - 179. [Abstract] [Full Text] [PDF]
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J. W. Scott Sniffing and Spatiotemporal Coding in Olfaction Chem Senses, February 1, 2006; 31(2): 119 - 130. [Abstract] [Full Text] [PDF]
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 S. B. Dietz and V. N. Murthy Contrasting short-term plasticity at two sides of the mitral-granule reciprocal synapse in the mammalian olfactory bulb J. Physiol., December 1, 2005; 569(2): 475 - 488. [Abstract] [Full Text] [PDF]
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T. A. Cleland and C. Linster Computation in the Olfactory System Chem Senses, November 1, 2005; 30(9): 801 - 813. [Abstract] [Full Text] [PDF]
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C. E. Reisenman, T. A. Christensen, and J. G. Hildebrand Chemosensory Selectivity of Output Neurons Innervating an Identified, Sexually Isomorphic Olfactory Glomerulus J. Neurosci., August 31, 2005; 25(35): 8017 - 8026. [Abstract] [Full Text] [PDF]
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 P.-M. Lledo, G. Gheusi, and J.-D. Vincent Information Processing in the Mammalian Olfactory System Physiol Rev, January 1, 2005; 85(1): 281 - 317. [Abstract] [Full Text] [PDF]
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H. Lei, T. A. Christensen, and J. G. Hildebrand Spatial and Temporal Organization of Ensemble Representations for Different Odor Classes in the Moth Antennal Lobe J. Neurosci., December 8, 2004; 24(49): 11108 - 11119. [Abstract] [Full Text] [PDF]
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 P.-M. Lledo, A. Saghatelyan, and M. Lemasson Inhibitory Interneurons in the Olfactory Bulb: From Development to Function Neuroscientist, August 1, 2004; 10(4): 292 - 303. [Abstract] [PDF]
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K. C. Daly, G. A. Wright, and B. H. Smith Molecular Features of Odorants Systematically Influence Slow Temporal Responses Across Clusters of Coordinated Antennal Lobe Units in the Moth Manduca sexta J Neurophysiol, July 1, 2004; 92(1): 236 - 254. [Abstract] [Full Text] [PDF]
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S. Nagayama, Y. K. Takahashi, Y. Yoshihara, and K. Mori Mitral and Tufted Cells Differ in the Decoding Manner of Odor Maps in the Rat Olfactory Bulb J Neurophysiol, June 1, 2004; 91(6): 2532 - 2540. [Abstract] [Full Text] [PDF]
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S. Lagier, A. Carleton, and P.-M. Lledo Interplay between Local GABAergic Interneurons and Relay Neurons Generates {gamma} Oscillations in the Rat Olfactory Bulb J. Neurosci., May 5, 2004; 24(18): 4382 - 4392. [Abstract] [Full Text] [PDF]
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K. R. Neville and L. B. Haberly Beta and Gamma Oscillations in the Olfactory System of the Urethane-Anesthetized Rat J Neurophysiol, December 1, 2003; 90(6): 3921 - 3930. [Abstract] [Full Text] [PDF]
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A. P. Davison, J. Feng, and D. Brown Dendrodendritic Inhibition and Simulated Odor Responses in a Detailed Olfactory Bulb Network Model J Neurophysiol, September 1, 2003; 90(3): 1921 - 1935. [Abstract] [Full Text] [PDF]
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D. A. Wilson Rapid, Experience-Induced Enhancement in Odorant Discrimination by Anterior Piriform Cortex Neurons J Neurophysiol, July 1, 2003; 90(1): 65 - 72. [Abstract] [Full Text] [PDF]
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J. Cang and J. S. Isaacson In Vivo Whole-Cell Recording of Odor-Evoked Synaptic Transmission in the Rat Olfactory Bulb J. Neurosci., May 15, 2003; 23(10): 4108 - 4116. [Abstract] [Full Text] [PDF]
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M. Wachowiak and L. B. Cohen Correspondence Between Odorant-Evoked Patterns of Receptor Neuron Input and Intrinsic Optical Signals in the Mouse Olfactory Bulb J Neurophysiol, March 1, 2003; 89(3): 1623 - 1639. [Abstract] [Full Text] [PDF]
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H. Hamana, J. Hirono, M. Kizumi, and T. Sato Sensitivity-dependent Hierarchical Receptor Codes for Odors Chem Senses, February 1, 2003; 28(2): 87 - 104. [Abstract] [Full Text] [PDF]
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C. Linster, B. A. Johnson, E. Yue, A. Morse, Z. Xu, E. E. Hingco, Y. Choi, M. Choi, A. Messiha, and M. Leon Perceptual Correlates of Neural Representations Evoked by Odorant Enantiomers J. Neurosci., December 15, 2001; 21(24): 9837 - 9843. [Abstract] [Full Text] [PDF]
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Z. Nusser, L. M. Kay, G. Laurent, G. E. Homanics, and I. Mody Disruption of GABAA Receptors on GABAergic Interneurons Leads to Increased Oscillatory Power in the Olfactory Bulb Network J Neurophysiol, December 1, 2001; 86(6): 2823 - 2833. [Abstract] [Full Text] [PDF]
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A. R. McQuiston and L. C. Katz Electrophysiology of Interneurons in the Glomerular Layer of the Rat Olfactory Bulb J Neurophysiol, October 1, 2001; 86(4): 1899 - 1907. [Abstract] [Full Text] [PDF]
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M. L. Schaefer, D. A. Young, and D. Restrepo Olfactory Fingerprints for Major Histocompatibility Complex-Determined Body Odors J. Neurosci., April 1, 2001; 21(7): 2481 - 2487. [Abstract] [Full Text] [PDF]
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 K. C. Daly, S. Chandra, M. L. Durtschi, and B. H. Smith The generalization of an olfactory-based conditioned response reveals unique but overlapping odour representations in the moth Manduca sexta J. Exp. Biol., January 9, 2001; 204(17): 3085 - 3095. [Abstract] [Full Text] [PDF]
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D. A. Wilson Comparison of Odor Receptive Field Plasticity in the Rat Olfactory Bulb and Anterior Piriform Cortex J Neurophysiol, December 1, 2000; 84(6): 3036 - 3042. [Abstract] [Full Text] [PDF]
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 K. Mori, H. Nagao, and Y. Yoshihara The Olfactory Bulb: Coding and Processing of Odor Molecule Information Science, October 22, 1999; 286(5440): 711 - 715. [Abstract] [Full Text]
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A. Didier, A. Carleton, J. G. Bjaalie, J.-D. Vincent, O. P. Ottersen, J. Storm-Mathisen, and P.-M. Lledo A dendrodendritic reciprocal synapse provides a recurrent excitatory connection in the olfactory bulb PNAS, May 22, 2001; 98(11): 6441 - 6446. [Abstract] [Full Text] [PDF]
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